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The genomic Echinococcus microsatellite EmsB sequences: from a molecular marker to the epidemiological tool

Published online by Cambridge University Press:  22 December 2009

J. KNAPP ,
J. M. BART ,
S. MAILLARD ,
B. GOTTSTEIN  and
R. PIARROUX
J. KNAPP
Affiliation:
Laboratory of Chrono-Environment, Department of Parasitology, UMR CNRS 6249, usc INRA, University of Franche-Comté, 19 rue Ambroise Paré, 25030Besançon, France Institute of Parasitology, Vetsuisse Faculty, University of Bern, Längass-Strasse 122, 3012Bern, Switzerland
J. M. BART
Affiliation:
Laboratory of Chrono-Environment, Department of Parasitology, UMR CNRS 6249, usc INRA, University of Franche-Comté, 19 rue Ambroise Paré, 25030Besançon, France
S. MAILLARD
Affiliation:
Laboratory of Chrono-Environment, Department of Parasitology, UMR CNRS 6249, usc INRA, University of Franche-Comté, 19 rue Ambroise Paré, 25030Besançon, France Institute of Parasitology, Vetsuisse Faculty, University of Bern, Längass-Strasse 122, 3012Bern, Switzerland
B. GOTTSTEIN*
Affiliation:
Institute of Parasitology, Vetsuisse Faculty, University of Bern, Längass-Strasse 122, 3012Bern, Switzerland
R. PIARROUX
Affiliation:
Laboratory of Chrono-Environment, Department of Parasitology, UMR CNRS 6249, usc INRA, University of Franche-Comté, 19 rue Ambroise Paré, 25030Besançon, France Department of Parasitology and Mycology, Hôpital la Timone, 13005Marseille, France
*
*Corresponding author: Institute of Parasitology, Vetsuisse Faculty, University of Bern, Längass-Strasse 122, 3012Bern, Switzerland. Tel: +41(31)6312476. Fax: +41(31)6312622. E-mail: bruno.gottstein@ipa.unibe.ch
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Summary

In the field of molecular and epidemiological parasitology, characterization of fast evolving genetic markers appears as an important challenge to consider the diversity and genetic structure of parasites. The study of respective populations can help us to understand their adaptive strategies to survive and perpetuate the species within different host populations, all trying to resist infection. In the past, the relative monomorphic features of Echinococcus multilocularis, the causative agent of alveolar echinococcosis and a severe human parasitic disease, did not stimulate studies dealing with the genetic variability of Echinococcus species or respective populations. A recently developed, characterized and validated original multilocus microsatellite, named EmsB, tandemly repeated in the genome, offered an additional opportunity for this line of investigation. We have compiled in this review new insights brought by this molecular tracker on the transmission activity of Echinococcus among different hosts and at different geographical scales.

Keywords

Echinococcus multilocularishighly polymorphic molecular markermicrosatellite EmsBpopulation dynamic activitytransmission patterneco-epidemiology
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 3: Development and applications of cestode and trematode laboratory models , March 2010 , pp. 439 - 449
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Bart, J. M., Abdukader, M., Zhang, Y. L., Lin, R. Y., Wang, Y. H., Nakao, M., Ito, A., Craig, P. S., Piarroux, R., Vuitton, D. A. and Wen, H. (2006 a). Genotyping of human cystic echinococcosis in Xinjiang, PR China. Parasitology 133, 571–579.CrossRefGoogle ScholarPubMed
Bart, J. M., Knapp, J., Gottstein, B., El-Garch, F., Giraudoux, P., Glowatzki, M. L., Berthoud, H., Maillard, S. and Piarroux, R. (2006 b). EmsB, a tandem repeated multi-loci microsatellite, new tool to investigate the genetic diversity of Echinococcus multilocularis. Infection, Genetics and Evolution 6, 390–400.CrossRefGoogle ScholarPubMed
Bartholomei-Santos, M. L., Heinzelmann, L. S., Oliveira, R. P., Chemale, G., Gutierrez, A. M., Kamenetzky, L., Haag, K. L. and Zaha, A. (2003). Isolation and characterization of microsatellites from the tapeworm Echinococcus granulosus. Parasitology 126, 599–605.Google ScholarPubMed
Bowles, J., Blair, D. and McManus, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.CrossRefGoogle ScholarPubMed
Bowles, J. and McManus, D. P. (1993). Molecular variation in Echinococcus. Acta Tropica 53, 291–305.CrossRefGoogle ScholarPubMed
Bretagne, S., Assouline, B., Vidaud, D., Houin, R. and Vidaud, M. (1996). Echinococcus multilocularis: microsatellite polymorphism in U1 snRNA genes. Experimental Parasitology 82, 324–328.CrossRefGoogle ScholarPubMed
Bretagne, S., Robert, B., Vidaud, D., Goossens, M. and Houin, R. (1991). Structure of the Echinococcus multilocularis U1 snRNA gene repeat. Molecular and Biochemical Parasitology 46, 285–292.CrossRefGoogle ScholarPubMed
Casulli, A., Bart, J. M., Knapp, J., La Rosa, G., Dusher, G., Gottstein, B., Di Cerbo, A., Manfredi, M. T., Genchi, C., Piarroux, R. and Pozio, E. (2009). Multi-locus microsatellite analysis supports the hypothesis of an autochthonous focus of Echinococcus multilocularis in northern Italy. International Journal for Parasitology 39, 837–842.CrossRefGoogle ScholarPubMed
Colwell, R. K. (2005). EstimateS: Statistical estimation of species richness and shared species from samples. Version 7.5. User's Guide and application published at: http://purl.oclc.org/estimates.Google Scholar
Eckert, J., Conraths, F. J. and Tackmann, K. (2000). Echinococcosis: an emerging or re-emerging zoonosis? International Journal for Parasitology 30, 1283–1294.CrossRefGoogle ScholarPubMed
Estoup, A., Jarne, P. and Cornuet, J.-M. (2002). Homoplasy and mutation model at microsatellite loci and their consequences for population genetic analysis. Molecular Ecology 11, 1591–1604.CrossRefGoogle Scholar
Gasser, R. B. and Chilton, N. B. (1995). Characterisation of taeniid cestode species by PCR-RFLP of ITS2 ribosomal DNA. Acta Tropica 59, 31–40.CrossRefGoogle ScholarPubMed
Guislain, M. H., Raoul, F., Giraudoux, P., Terrier, M. E., Froment, G., Ferte, H. and Poulle, M. L. (2008). Ecological and biological factors involved in the transmission of Echinococcus multilocularis in the French Ardennes. Journal of Helminthology 82, 143–151.CrossRefGoogle ScholarPubMed
Haag, K. L., Araujo, A. M., Gottstein, B. and Zaha, A. (1998). Selection, recombination and history in a parasitic flatworm (Echinococcus) inferred from nucleotide sequences. Memorias do Instituto Oswaldo Cruz 93, 695–702.CrossRefGoogle Scholar
Haag, K. L., Zaha, A., Araujo, A. M. and Gottstein, B. (1997). Reduced genetic variability within coding and non-coding regions of the Echinococcus multilocularis genome. Parasitology 115, 521–529.CrossRefGoogle ScholarPubMed
Kern, P., Bardonnet, K., Renner, E., Auer, H., Pawlowski, Z., Ammann, R. W. and Vuitton, D. A. (2003). European echinococcosis registry: human alveolar echinococcosis, Europe, 1982–2000. Emerging Infectious Diseases 9, 343–349.CrossRefGoogle ScholarPubMed
Knapp, J. (2008). Caractérisation et validation du marqueur microsatellite multilocus répété en tandem EmsB pour la recherche de polymorphisme génétique chez Echinococcus multilocularis: Application à l'étude de la transmission du parasite en Europe. PhD Thesis, University of Franche-Comté.Google Scholar
Knapp, J., Bart, J. M., Giraudoux, P., Glowatzki, M. L., Breyer, I., Raoul, F., Deplazes, P., Duscher, G., Martinek, K., Dubinsky, P., Guislain, M. H., Cliquet, F., Romig, T., Malczewski, A., Gottstein, B. and Piarroux, R. (2009). Genetic diversity of the cestode Echinococcus multilocularis in red foxes at a continental scale in Europe. PLoS Neglected Tropical Diseases 3, e452.CrossRefGoogle Scholar
Knapp, J., Bart, J. M., Glowatzki, M. L., Ito, A., Gerard, S., Maillard, S., Piarroux, R. and Gottstein, B. (2007). Assessment of microsatellite polymorphism for improving the spatial distribution tracking of Echinococcus multilocularis. Journal of Clinical Microbiology 45, 2943–2950.CrossRefGoogle ScholarPubMed
Knapp, J., Guislain, M. H., Bart, J. M., Raoul, F., Gottstein, B., Giraudoux, P. and Piarroux, R. (2008). Genetic diversity of Echinococcus multilocularis on a local scale. Infection, Genetics and Evolution 8, 367–373.CrossRefGoogle ScholarPubMed
Lavikainen, A., Lehtinen, M. J., Meri, T., Hirvela-Koski, V. and Meri, S. (2003). Molecular genetic characterization of the Fennoscandian cervid strain, a new genotypic group (G10) of Echinococcus granulosus. Parasitology 127, 207–215.CrossRefGoogle Scholar
Legendre, P. and Legendre, L. (1998). In Numerical Ecology, 2nd English edition. Elsevier Science BV, Amsterdam.Google Scholar
Maillard, S., Gottstein, B., Haag, K., Ma, S., Colovic, I., Benchikh-Elfegoun, M. C., Knapp, J., and Piarroux, R. (2009). The tandemly repeated multilocus microsatellite EmsB: a new tool to investigate the genetic diversity of Echinococcus granulosus sensu lato. Journal of Clinical Microbiology. Epub ahead of print.CrossRefGoogle ScholarPubMed
Monis, P. T., Andrews, R. H. and Saint, C. P. (2002). Molecular biology techniques in parasite ecology. International Journal for Parasitology 32, 551–562.CrossRefGoogle ScholarPubMed
Nakao, M., McManus, D. P., Schantz, P. M., Craig, P. S. and Ito, A. (2007). A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134, 713–722.CrossRefGoogle ScholarPubMed
Nakao, M., Sako, Y. and Ito, A. (2003). Isolation of polymorphic microsatellite loci from the tapeworm Echinococcus multilocularis. Infection, Genetics and Evolution 3, 159–163.CrossRefGoogle ScholarPubMed
Okamoto, M., Oku, Y., Kurosawa, T. and Kamiya, M. (2007). Genetic uniformity of Echinococcus multilocularis collected from different intermediate host species in Hokkaido, Japan. Journal of Veterinary Medical Science 69, 159–163.CrossRefGoogle ScholarPubMed
Posselt, A. (1900). Die geographische Verbreitung des Blasenwurmleidens insbesondere des Alveolarechinokokkus des Leber und dessen Casuistik seit 1886. Enke, Stuttgart.Google Scholar
Ricklefs, R. E. and Miller, G. L. (2000). In Ecology W. H. Freeman, New York.Google Scholar
Rinder, H., Rausch, R. L., Takahashi, K., Kopp, H., Thomschke, A. and Loscher, T. (1997). Limited range of genetic variation in Echinococcus multilocularis. Journal of Parasitology 83, 1045–1050.CrossRefGoogle ScholarPubMed
Roratto, P. A., Bartholomei-Santos, M. L., Gutierrez, A. M., Kamenetzky, L., Rosenzvit, M. C., and Zaha, A. (2006). Detection of genetic polymorphism among and within Echinococcus granulosus strains by heteroduplex analysis of a microsatellite from the U1 snRNA genes. Genetics and Molecular Research 5, 542–552.Google ScholarPubMed
Saarma, U., Jogisalu, I., Moks, E., Varcasia, A., Lavikainen, A., Oksanen, A., Simsek, S., Andresiuk, V., Denegri, G., Gonzalez, L. M., Ferrer, E., Garate, T., Rinaldi, L. and Maravilla, P. (2009). A novel phylogeny for the genus Echinococcus, based on nuclear data, challenges relationships based on mitochondrial evidence. Parasitology 136, 317–328.CrossRefGoogle ScholarPubMed
Scott, J. C., Stefaniak, J., Pawlowski, Z. S. and McManus, D. P. (1997). Molecular genetic analysis of human cystic hydatid cases from Poland: identification of a new genotypic group (G9) of Echinococcus granulosus. Parasitology 114, 37–43.CrossRefGoogle ScholarPubMed
Smith, J. E. (2009). Chapter 6. Tracking Transmission of the Zoonosis Toxoplasma gondii. Advances in Parasitology 68, 139–159.CrossRefGoogle Scholar
Takumi, K., de Vries, A., Chu, M. L., Mulder, J., Teunis, P. and van der Giessen, J. (2008). Evidence for an increasing presence of Echinococcus multilocularis in foxes in The Netherlands. International Journal for Parasitology 38, 571–578.CrossRefGoogle ScholarPubMed
Templeton, A. R. (2008). The reality and importance of founder speciation in evolution. Bioessays 30, 470–479.CrossRefGoogle ScholarPubMed
Thompson, R. C. and McManus, D. P. (2002). Aetiology: parasites and live-cycles. In: WHO/OIE Manuel on echinococcosis in humans and animals: a public health problem of global concern (ed. Eckert, J., Gemmell, M. A., Meslin, F. X. and Pawlowski, Z. S.), pp. 1–19. World Organization for Animal Health, Paris, France.Google Scholar
van Herwerden, L., Gasser, R. B. and Blair, D. (2000). ITS-1 ribosomal DNA sequence variants are maintained in different species and strains of Echinococcus. International Journal for Parasitology 30, 157–169.CrossRefGoogle ScholarPubMed
Vuitton, D. A., Zhou, H., Bresson-Hadni, S., Wang, Q., Piarroux, M., Raoul, F. and Giraudoux, P. (2003). Epidemiology of alveolar echinococcosis with particular reference to China and Europe. Parasitology 127 (Suppl), S87–S107.CrossRefGoogle ScholarPubMed
Yang, Y. R., Rosenzvit, M. C., Zhang, L. H., Zhang, J. Z. and McManus, D. P. (2005). Molecular study of Echinococcus in west-central China. Parasitology 131, 547–555.CrossRefGoogle ScholarPubMed